shark Carcharhinus amblyrhynchos in Hawaii

MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
!
h b l i s h e d May 22
Distribution, reproduction and diet of the gray reef
shark Carcharhinus amblyrhynchos in Hawaii
Bradley M. W e t h e r b e e 1 , * , Gerald L. Crow2, Christopher G. Lowel
'Zoology Department, 2538 The Mall, University of Hawaii, Honolulu, Hawaii 96822, USA
2 ~ a i k i kAquarium,
i
2777 Kalakaua Ave., Honolulu, Hawaii 96815, USA
ABSTRACT- Distribution, reproduction, and diet of the gray reef shark Carcharhinos arnblj.rhynchos
were investigated using data collected during shark control programs in the main Hawdiian Islands
(MHI) and during research fishing in the Northwestern Hawaiian Islands (NWHI).A total of 472 sharks
were caught between 1967 and 1980. These sharks have a restricted distribution in the MHI; they were
collected only in the vicinity of Niihau and Molokini islands, but were one of the most abundant sharks
throughout the NWHl. Catch rate was higher for males than for females in standard longline fishing at
all locations and dunng all seasons. Most shdrks were caught at depths between 20 and 6 0 m, and
depth distribution of the sexes was similar, although females were more common at shallower depths.
hlales ranged in size from 7 9 to 185 cm total length (TL), and matured at between 120 and 140 cm TL.
Females ranged in size between 6 3 and 190 cm TL and matured at about 125 cm TL. Litter size ranged
from 3 to 6 , with an average of 4.1 pups. Size a t birth was estimated to be just over 6 0 cm TL. Most
sharks (85%) consumed teleosts, but some fed on cephalopods (29.5'%),and crustaceans (4.9%). For
sharks in the largest size classes, the frequency of occurrence of teleosts declined, whereas that of
cephalopods ~ncreased.
K E Y WORDS Gray reef shark . Hawaii Distribution . Keproductlon . D ~ e t
INTRODUCTION
The gray reef shark Carcharhinus amblyrhynchos is
widely distributed in the Indian, and western and central Pacific Oceans, ranging from the eastern coast of
southern Africa, to the Hawaiian and Tuamotu archipelagos (Garrick 1982, Compagno 1984). This shark is
common on outer reef slopes of islands and continents,
as well as in lagoons and passes to the open ocean
(Hobson 1963, McKibben & Nelson 1986). I t is distinguished from other carcharhinids by the absence of an
interdorsal ridge, and the presence of a conspicuous
black margin on the trailing edge of the caudal fin
(Johnson 1978, Gal-rick 1982). However, Compagno
(1984) suggested that the very similar appearing black
tail reef shark Carcharhinus wheeler] may be a synonym of C. amblyrhynchos.
8 Inter-Research 1997
Resale of full artjcle not permitted
The gray reef shark has attained a reputation for
aggressiveness and has been responsible for a number
of attacks on humans (Hobson et al. 1961, Fellows &
Murchison 1967, Read 1971). Not surprisingly, most
studies have concentrated on behavioral aspects, such
as feeding (Hobson 1963),activity patterns (McKibben
& Nelson 1986), and agonistic display (Johnson & Nelson 1973, Barlow 1974, Nelson 1982, Nelson et al.
1986). Age and growth of this shark have also been
investigated (DeCrosta et al. 1984, Radtke & Cailliet
1984). This species forms part of the shark fishery in
Thailand, and is caught for flesh and fins in other locations (Compagno 1984, Last & Stevens 1994). Despite
its wide distribution, use in scientific studies, and
occurrence in fisheries, very little is known about the
life history of C. amblyrhynchos.
The gray reef shark is one of the most abundant
sharks in the low, remote, largely uninhabited, Northwestern Hawaiian Islands (NWHI), and also occurs in
the main Hawaiian Islands (MHI) (Wass 1971,
MarEcolProg Ser 151 181-189, 1997
182
DeCrosta et. al. 1984). The purpose of this study is to
provide information on the distribution, reproduction,
and diet of the gray reef shark based on data collected
from sharks captured during fishing programs in
Hawaii.
ered low (0-0.29), medium (0.3-0.59), or high (>0.6),
following Langton (1982) Prey diversity of each of the
3 size classes was calculated using the ShannonWeiner Diversity Index (H')(Krebs 1989).
RESULTS
METHODS
Distribution
Most of the data used in this study came from original data sheets of the Hawaii Cooperative Shark
Research and Control Program, which ran from 1 June
1967 through 30 J u n e 1969 (Tester 1969). In this program, sharks were captured using standard longlines,
light-tackle longlines (12 hooks), and handlines. Standard longlines consisted of three 800 m sections, 24
hooks per section. Lines with hooks baited primarily
with skipjack tuna Katsuwonus pelamis were set late
in the afternoon, parallel to shore, in depths averaging
45 m , and were retrieved the following morning. Fishing was conducted from a tuna fishing boat in designated areas around the 8 MHI (Wetherbee et al. 1994).
Sharks were also captured during control programs
that operated in the MHI in 1971 a n d 1976 (see
Wetherbee et al. 1994).Data collected for sharks captured with longlines, handlines, and by spearfishing in
the NWHI between 1978 and 1980 (DeCrosta et al.
1984) were also examined. Additional data came from
sharks captured a t Enewetak Atoll and Johnston Atoll
(see Wass 1971). The data from both atolls was combined since the exact site of capture was not differentiated.
Depth of capture, precaudal length (PCL), total
length (TL), sex, and weight (occasionally) were
recorded for each shark. All lengths in this study refer
to TL. For males, the length and degree of calc~fication
of claspers were noted, and for females, the diameter
of the 6 largest ova and uterus width were measured.
The number, sex, and TL of embryos in pregnant
females were also recorded. We classified males with
elongate ( > l 2 0 mm) and calcified claspers as mature,
and those with small uncalcified claspers a s immature.
Females with large developing ova and large uteri
were classified a s mature, whereas those with small
ova (<S mm) and thin uteri ( c 5 mm) were classified as
immature. Some small sharks were measured, tagged
and released in the MHI.
Stomach contents were identified to the lowest possible taxa and were quantified on the basis of percentage of occurrence: (number of stomachs that contained
a prey i t e m h u m b e r of stomachs that contained food) X
100. Dietary overlap was calculated for small (50100 cm), medium (100-150 cm) and large (150200 cm) size classes using the Simplified Morisita
Index (ClI ) (Krebs 1989). Degree of overlap was consid-
A total of 367 gray reef sharks were caught in
Hawaii, 277 from the MHI and 90 from the NWHI
(Table 1). All but 3 of these sharks from the MHI were
captured during the 1967 to 1969 Hawaii Cooperative
Shark Research and Control Program. The other 3 MHI
sharks were captured in the smaller-scale shark control programs conducted in 1971 and 1976. Only limited data were available for 105 sharks captured at
Johnston and Enewetak atolls. Almost all sharks from
the MHI were captured at either Niihau or Molokini.
By far the largest number of sharks (189) was captured
at Niihau, a low island located at the northern end of
the MHI, which is inhabited by only a few hundred
native Hawaiians (Fig. 1). Thirty-six sharks were
caught at Ka'ula Rock, a small island located 40 km SW
of Niihau, and 45 sharks were caught a t Moloklni, the
remnant of a small crater near the island of Maui.
In longline fishing in the MHI, the highest catch
rates were at Molokini. Ka'ula Rock, and Niihau
(Table 1). The overall longline catch rate was 0.32
sharks/100 hooks, and for only those areas where gray
reef sharks were captured, the rate was 1.52 sharks/
100 hooks (on 4673 hooks). Although the majority of
fishing in the MHI was conducted in waters surrounding the island of Oahu, not a single gray reef shark was
caught on 11905 longline hooks set near this island
(see Wetherbee et al. 1994). However, Wass (1971)
reported that several gray reef sharks were captured
off Oahu in other fishing
The composition of catches in the MHI varied with
gear used. Of 71 sharks captured on longlines, 40 were
mature (31 males 9 females), and 26 were immature
(15 males l 1 females) In handl.ine flshing, all but 4 of
179 sharks caught were immature. Niihau was the only
location where a large number of mature sharks was
ca.ptured with either gear (37 sharks). In areas where
sharks were abundant, immature sharks were caught
more frequently than mature sharks (Table 1)
In the NWHI, sharks were caught virtually everywhere that fishing was conducted (Table 1).In longline
fishing, the highest catch rates were at Necker Island
(although only 16 hooks were set) and French Frigate
Shoals. The overall catch rate of 8.78 sharks per 100
hooks for the NWHI was substantially higher than for
the MHI. Again, longline fishing resulted in the cap-
Wetherbee et al.: Life history of the gray reef shark
183
-
Table 1 C a ~ c h a r h l n u sarnblyrhynchos Numbers of hooks set sharks caught, and catch pel unit e f f o ~ tCPUE (sharks per 100
hooks] at locat~onswhere grav rerf sharks were captured In the rnaln Hawallan Islands (LIHI), Northwestern Ha\zra~~an
Islands
(NWHI),and Johnston and Enewetak atolls on longl~nes(LL)and handhnes (HL) F females. M males. FFS Frcnch F r ~ g a t eShoc~ls
Locatlon
No of LL hooks
F
Matu~e
M
Immature
F
M
Unknown
Total
p
-
P
MHI
Ni~hau
LL
HL
LL
HL
Ka ula Rock
LL
Kaua~
Maul
h4olok1n1
LL
LL
2020
168
Kaho olawe
Hawall
Totd
LL
LL
WHI
Midway
LL
HL
LL
HL
LL
FFS
Maro Reef
709
72
63
3
3
0
152
1489
4673
6
56
0
16
0
1
4
20
0
0
103
10
60
3
9
0
0
2
14
10
0
0
0
0
0
1
0
34
0
0
0
0
3
8
4
32
3
0
1
0
2
0
0
1
0
0
0
98
2
18
1
4
1
0
0
5
0
1
32
6
131
0 07
1 52
2
0
0
0
0
0
0
0
HL
0
0
2
2
0
4
18
38
17
11
6
90
51
33
10
7
4
105
1
6
0
80
2
l
0
0
4
0
2
16
0
0
2
0
0
0
0
0
HL
2
558
l
4 17
39
2
1
277
HL
383
7
2 52
0 42
1 39
9 52
HL
79
Johnston & Enewetak atolls
Midway I
L>
51
138
7
29
3
1
0
0
0
3
0
1
0
1
0
1
LL
Laysan
Pearl & Hermes
N~hoa
Total
27
1
0
1 ]L
Necker
6
0
HL
'"$'
CPUE
4
13
5 06
40
11
10 44
3
7
3 75
2
3
12 5
2
l
8 78
29"
I
. 3 ~ e a rand
l Hermes Reef
1
l
-25"
.20"
18'
Fig. 1. Map of the Hawaiian Archipelago
Mar Ecol Prog Ser 151: 181-189, 1997
184
Mature
Mature
V)
4I1
I Males (n=64)
[U Females (11.26)
2.5
30
II
a
V."
Spr~ng
(610)
Summer
Fall
(1443)
(839)
W~nter
(153)
Immature
1I11
'""
In
2.5
0
W Males (n=18)
Females (n=l3)
bl
1
1
Immature
0
=
2.0-
0
0
7-
L
1.5-
a,
",
Q.
5m
1.00.5-
V)
0.0
Spring
Summer
Fall
Winter
(610)
(1443)
(839)
(153)
Season
-.
Fig. 2. Carcharhlnus amblyrhynchos. Catch rate (sharks per
100 hooks) dunny diffe~entseasons for gray reef sharks
captured in longline fishing in the main Hawailan Islands.
(a] Mature sharks; (b) immature sharks. Numbers in parentheses are hooks set during each season
ture of primarily mature sharks (45 of 49 sharks were
mature), with a predominance of males (35 males,
10 females). For sharks captured by handline or spear,
11 were mature and 24 were immature. In contrast to
Hawaii, fewer mature males than females were caught
at Enewetak and Johnston atolls (Table 1).
In the MHI, the catch rate of mature males on longlines was relatively constant throughout the year, but
was more variable for mature females, a n d no mature
females were captured in winter (Fig. 2a). Sample size
for immature sharks was small, but catch rates for
males were also higher than for females (Fig 2b)
Although the depth ranges of capture for mature
males a.nd females largely overlapped, there is some
indication that males occurred at greater depths
(Fig. 3a). Sixteen of 19 mature sharks captured at
depths of less than 10 m were females, whereas 14 of
the 17 mature sharks captured deeper than 50 m were
males. The majority of immature sharks of both sexes
Depth (m)
-
,-
Fig. 3. Carcharhinus amblyrhynchos. Numbers of gray reef
sharks captured at 10 m depth intervals in longllne fishing in
Hawaii. (a) Mature sharks; (b) immature sharks
were captured at depths between 20 and 60 m
(Fig 3b). The average depth ( & lSD) of capture for
mature females was 22.2 m i 15.8 (range = 1 to 91. m,
n = 61); for mature males, 36.2 m t 20.0 (range = 5.5 to
106.1 m , n = 72); for immature females, 37.1 & 13.4
(range = 5.5 to 73.2 m, n = 111); and for immature
males, 39.3 t 12.8 (range = 11.0 to 80.5 m, n = 3 11).
Reproduction
Since total length measurements tend to be more
variable when different observers take measurements,
a linear regression was used to convert PCL to TL (in
cm):
TL = 4.146 + 1.262PCL (r2= 0.995, n = 409)
A length-frequency histogram for all sharks examined showed that more sharks in the larger size classes
Wetherbee et al. L ~ f ehistory of the gray reef shark
-
7
1 W Males (n-219)
Z
.
i
70 '
-
Females (n=208)
I
Total Length (cm)
Fig. 4. Carcharhinus amblyrhynchos. Length frequency histogram for male and female gray reef sharks from Hawaii, and
Johnston and Enewetak atolls
185
-
119 cm, and short, uncalcified claspers were recorded
for males up to 140 cm.
For females there was a rapid increase in the development of the uterus for sharks just over 125 cm TL
(Fig 7). All females shorter than 125 cm TL had uteri
less than 5 mm in diameter, and all females longer than
127 cm TL had uteri larger than 15 mm in diameter
Maximum ova diameter was measured for only 8
females, a n d did not reveal ti.me of ovulation. The data
gathered allowed only limited inference of seasonality
of reproduction. Mating scars were noted on only 1
individual, which was captured in March. Very small
embryos (average 2.5 cm) were observed in uteri of a
pregnant female also caught in March. However, eggs
were observed in uteri of a female captured in July in
the NWHI.
m
calcified (n=91)
o
females (n=115)
W = 1.36
a
males (n=108)
W
X
,7.07 X
10-06 T L ~ .r2 ~= 0.976
~
10-07 ~ ~ 3 . 4 r2
6
= 0.939
"1
40
Total Length (cm)
Fig. 6 . Carcharhinus amblyrhynchos. Clasper length versus
total length of male gray reef sharks captured in fishing in
Hawaii
Total Length (cm)
Flg. 5. Carchal-hjnus anlblyrhynchos Length-weight relat~onship for male dnd female gray reef sharks captured In Hawaii.
Solid line: females, dashed line: males
were males, 1,vhereas there were more females in the
smaller size classes (Fig. 4 ) . A peak in numbers in the
76-100 cm size class was apparently due to the large
number of small sharks captured with handlines. The
largest female captured was 190 cm, and the largest
male was 185 cm (and only 1 other male was greater
than 170 cm).The sex ratio of males to females differed
significantly from unity (x2 = 264.1, p = 0.001, n = 326).
The length-weight relationships were similar for the
2 sexes (Fig. 5).
As males reached 120 cm, there was a rapid increase
in the length and degree of calcification of the claspers
(Fig. 6). The sn~allestmale with calcified claspers was
Total Length (cm)
Fig. 7 Carcharhinus amblyrhynchos. Uterus width versus
total length of female gray reef sharks captured In fishing in
Hawaii
Mar Ecol Prog Ser 151. 181-189, 1997
Fourteen of 29 (48.3 %) mature females captured in
Hawaii and examined internally were pregnant. These
pregnant females ranged in size from 14 to 183 cm
(n = 14), whereas those from Johnston a n d Enewetak
were between 133 a n d 157 cm (n = 19). Between 3 and
6 embryos were found in pregnant females from
Hawaii (average 4.1, SD = 1.44, n = 13), whereas
females from Johnston a n d Enewetak contained
between 1 and 4 embryos (average 2.5, SD = 0.96, n =
19). A regression analysis showed little association
between TL of pregnant females and the number of
pups in uteri (r2 = 0.22).Embryos from Hawaii ranged
in si.ze from 2.5 cm (March) to 39.2 cm (November),
a n d the largest from JohnstonEnewetak averaged
49.6 cm (date unknown). A 63 cm shark captured in
July h a d a visible umbilical scar a n d was the smallest
free-swimming shark caught in Hawaii. The next
smallest individuals were 4 sharks (65 to 67 cm) captured between July and November.
Of 113 sharks tagged, l l (9.7 %) were recaptured, all
in close proximity to the tagging sites. Time at liberty
ranged from 3 to 566 d (average = 200 d). Total length
of tagged sharks averaged 85 cm, a n d ranged from
65 cm to 138 cm. Only 6 of the 11 sharks recaptured
showed positive growth, which averaged 3.9 cm yr-',
based on increase in PCL.
Table 2. Cdrcharhin~~s
amblyrhynchos. Stomach contents of
3 classes of gray reef sharks collected In the Hawaiian Islands,
expressed as percentage of occurrence. Lengths are total lengths
in cm. Of 153 stomachs examined, 61 contained food (39.9%)
Diet
tained cephalopods (29.5%) a n d crustaceans (4.9%)
(Table 2). In terms of frequency of occurrence, there
was an decrease for teleosts, and a n increase for
cephalopods for sharks in the largest 2 size classes
(Fig. 8 ) . Only stomachs of sharks in the largest size
class contained undigestible items. The Simplified
Morisita Index of dietary overlap (CH)revealed a low
degree of overlap between small and medtum size
sharks (C,, = 0.25), a n d between small and large sharks
(CII= 0.20). For the medium a n d large size classes, CH
was high (0.66).The Shannon-Weiner Index of dietary
diversity (H') was similar for all size classes, but
increased from 0.54 for the smallest size class, to 0.70
for the medium size sharks, a n d 0.71 for the largest
sharks.
Of 153 stomachs examined, 61 (39.9%) contained
food. The diet of sharks of all slze classes was dominated by teleost fishes ( 8 5 . 2 % ) ,but stomachs also con-
50-100
Teleostei
Muraenidae
Holocentridae
Scorpaenidae
Chaetodontidae
Pomacentridae
Scaridae
Zanclidae
Acanthuridae
Monacanthidae
Unidentified
Cephalopoda
Octopus
Squid
Unidentified
Crustracea
Lobster
Shrimp
Unidentified
Undigestible
Empty
100-150
150-200
(n = 4 4 )
87.5
0
18.8
0
6.3
0
0
0
0
0
56.2
66.7
9.1
0
3.0
0
3.0
0
3.0
0
0
48.5
61.5
0
0
0
0
0
3.8
0
7.7
77
42 3
85.2
4.9
4.9
1.6
1.6
1.6
1.6
1.6
33
33
59.0
6.2
6.2
0
0
30.3
26.1
3.0
6.1
26.9
15.4
7.7
29.5
18.0
4.9
6.6
6.2
0
0
6.2
3.0
3.0
0
0
3.8
0
3.8
0
4.9
1.6
1.6
1.6
0
0
63.6
43.1
cm
Total
cm
(n = 58)
cm
(n = 51)
7.7
7.7
3.3
49.0
60.1
DISCUSSION
Distribution
Fig. 8. Carchartunus amblyrhynchos. Percentage of occurrence of prey items in stomachs of 3 size classes of gray reef
sharks caught In Hawaii. Numbers abocc columns are sample
sizes for each size class
The gray reef shark was the third most common
shark captured in fishing programs in Hawaii, exceeded only by the sandbar Carcharhinus plumbeus
and ti.ger Galeocerdo cuvier sharks (Wetherbee et al.
1994).However, the number of gray reef sharks caught
on longlines was low in comparison to other species,
Wetherbee et al.. Life hi story of the gray reef shark
and large catches on handlines in a few fishing areas
greatly increased the number captured.
Capture of sharks at only a few locations, despite
longline sets of over 20000 hooks in the MHI, illustrates the rarity of this species, and suggests that other
species of sharks are frequently misidentifled as gray
reef sharks by SCUBA divers and others in Hawaii. It is
poss~blethat catch rates were low because little fishing
was conducted in habitats preferred by gray reef
sharks (outer reef slopes and steep dropoffs), but this
shark is rarely observed in these areas by knowledgeable divers (R. Pyle pers. comm., R. Kosaki pers.
comm.).
The scarcity and patchy distribution of gray reef
sharks in the high, populated, MHI in contrast to their
cosmopolitan presence in the low, unpopulated NWHI,
raises a number of questions about determinants of
their geographical distribution. Similar differences in
abundance of gray reef sharks at small, low, islands
and atolls in contrast to larger, high islands has been
suggested for other parts of the Pacif~c(Johnson 1978,
McKibbben & Nelson 1986).
Several factors might influence the distribution of
this species on a local scale. Differences in underwater
topography at different types of islands is one possibility, since this shark is thought to be bottom-oriented,
and to prefer areas of rugged terraln, strong currents,
and the leeward sides of islands (Hobson 1963, Wass
1971, Johnson 1978). Coral cover, and associated
ecosystem structure, is another potential factor since
coral reefs are generally less developed at younger,
high islands in comparison to older, low islands a n d
atolls. Water temperature and oceanographic effects of
high islands on the surrounding waters may also influence distribution. Large human populations (which
more commonly occur at high islands) may affect distribution through such factors as habitat degradation
and fishing pressure. For example, Wass (1971) suggested that this shark prefers clear water, and that
waters surrounding islands with large human populations tend to be more turbid. Competition between
gray reef sharks and other species is another possibility Wass (1971) theorized that Galapagos Gal-charhlnus galapagensis and sandbar sharks were spat~ally
segregated within Hawaii, and Kato & Carvallo (1967)
found that Galapagos sharks were segregated from sllvertip sharks C. albimarginatus at Socorro Island.
Comparison of resource overlap between the gray reef
shark and sympatric carcharhinids may reveal evidence of competition.
The very localized abundance of gray reef sharks at
Molokini (the only area in the lower MHI where they
were common) is striking. They a r e now rarely
observed at Molokini (J. Randall pers. comm., M. Severns pers. comm.). The patchy distribution and site
187
fidelity (as indicated by tag and recapture sites) of this
shark has apparently contributed to its having been
fished out at Molokini, and suggests that local populations may be quickly decimated by modest fishing
pressure.
Segregation of sharks by sex or age group has been
observed in many species, Including several species in
Hawaii (Wetherbee et al. 1994, Wetherbee et al. 1996).
There is also evidence of sexual segregation in the
gray reef shark. The capture of 3 times as many mature
males (average depth of capture 36.2 m) as mature
females (average depth of capture 22.2 m) supports the
contention that males tend to occur at greater depths,
since most longline fishing was conducted at about
45 m. The fluctuating catch rate of mature females may
reflect seasonal movement of females out of fishing
areas a n d into shallow-water, nursery areas. Large
aggregations of mature females [some pregnant) have
been observed in water only a few meters deep in the
NWHI and at Johnston Atoll (Taylor 1994, A. Econilnakis pers. comm.).There is also evidence of segregation of gray reef sharks by size class In Hawaii. Catches
at Molokini and Ka'ula Rock were composed almost
exclusively of juveniles, and these locations may serve
(or have served) as nursery areas. In general, low catch
rates for this species in the MHI l ~ m i tour understanding. of distri'butional patterns, although it is clear that
these sharks have a restricted distribution in the MHI,
and are uncommon near islands with large human
populations.
Reproduction
Although Garrick (1982) described what was possibly a 254 cm male Cal-charhinus amblyrhynchos, and
Schultz et al. (1953) reported a 232 cm female, the
largest sharks captured in Hawaii were considerably
smaller. Wass (1971)suggested that this shark attains a
larger size in Hawaii than elsewhere, but the largest
(190 cm) of the nearly 400 specimens captured in
Hawaii is similar to maximum sizes reported from
other locations (Johnson 1978, Stevens & McLoughlin
1991, Last & Stevens 1994).
Examination of the development of reproductive
structures of large numbers of sharks revealed that
males mature at between 120 a n d 140 cm, and females
at just over 125 cm in Hawaii. Other estimates of size at
maturity have ranged between 130 a n d 150 cm for
both sexes (Fourmanoir 1976, McKibben & Nelson
1986, Stevens & McLoughlin 1991). Based on growth
rates of both captive and wild sharks, this corresponds
to an a g e at maturity of 6 to 8 yr [Wass 1971, Radtke &
Cailliet 1984), although Fourmanoir (1976) estimated
that maturity was attained in as little as 3 yr
188
Mar Ecol Prog Ser 151. 181-189. 1997
Sizes of the smallest pregnant femalv in Hawaii
(141cm) and at Johnston and Enewetak (i33cm) were
similar to those recorded from other locations (Bonham
1960,McKibben & Nelson 1986,Stevens & McLoughlin 1991).Based on the timing of mating scars and
small embryos in uteri of females, and semen in seminal vesicles of males, mating and fertilization appear to
occur between March and May in Hawaii, possibly
continuing until July.
Based on the capture of females with 'near full-term
pups', and small, free-swimming sharks (most with
umbilical scars), pupping also appears to occur
between March and July, with a n apparent gestation
period of 12 mo. However, small, free-swimming
sharks were captured as late as November, and Nelson
(pers. comm.) caught females with what he considered
'full term' embryos during the fall at Enewetak. The
observation that approximately 50% of mature females
captured were pregnant suggests that females reproduce every other year There is little information In the
literature on the reproductive cycle of this shark for
comparison, other than speculation that in the southern hemisphere, parturition occurs in July and August,
and gestation is between 9 and 12 mo (Fourmanoir
1976,Johnson 1978,Stevens & McLoughlin 1991).
The smallest free-swimming shark caught in Hawaii
(63 cm) was similar in size to those recorded from other
locations, and agrees with an estimated size a t birth of
60 cm (Garrick lgg2,
&
However, free-swimming sharks as small as 42 cm (Johnson
1978,Salini et al. 1992)and embryos as large as 64 cm
(Stevens & McLoughlin 1991) have been examined.
Litter size of sharks in Hawaii (average of 4.1)may be
larger than in other locations, including the Johnston/
Enewetak females (average of 2.5).Most studies have
reported litter sizes between 1 and 4 (Schultz et al.
1953, Bonham 1960, Fourmanoir 1976, Stevens &
McLoughlin 1991).The average growth rate of gray
reef sharks tagged in Hawaii (3.9cm yr-l, based only
on sharks that showed positive growth) was greater
than previous estimates from this data (Tester 1969,
Wass 1971) However, our estimate is still low in comparison to other studies, which have ranged from 9 to
25 cm yr-' (Fourmanoi.r 1976,Johnson 1978,DeCrosta
et al. 1984,Radtke & Cailliet 1984).
Diet
The finding that gray reef sharks in Hawaii feed primarily on teleosts, supplemented by invertebrates, is
consistent with other reports. Jn previous studies, 65 to
88% of stomachs contained fish, and less than 25% of
stomachs contained either cephalopods or crustaceans
(Johnson 1978,Salini et al. 1990,Brewer et al. 1991).In
our study, the majority of prey items found in stomachs
were reef-associated and benthic organisms, indicating that sharks primarily fed near the bottom. Ontogenetic changes in the type and diversity of prey consumed by the gray reef shark is consistent with reports
for a number of other species of sharks (Wetherbee et
al. 1990,1996.Lowe et al. 1996).
CONCLUSIONS
Even th.ough most of these data are nearly 30 yr old,
they still represent an important contribution toward
understanding the distribution, reproduction and diet
of this species in Hawaii and throughout its range. An
example of the usefulness of this information came in
1992,when a bill was introduced to the state legislature of Hawaii calling for eradication of sharks that
pose a threat to humans. Among the species proposed
to be targeted for such shark control efforts was the
gray reef shark. Given that these sharks appear to be
exceedingly rare in Hawaiian waters frequented by
humans, directed fishing for this species for purposes
of protection of humans was deemed to be unwarranted.
Acknowledgements. We thank M. DeCrosta, J . Parrish, L.
Taylor Jr, A . Tester, R. Wass, and others for collecting the
data K. Holland, C. Mostello. D. Nelson, J . Parrish, and J .
Randall offered helpful comments on the manuscript. Thls
study is dedicated to the memory of D. Nelson.
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This a r t ~ c l ewas submitted to the editor
A4an uscnpt first received: N o v e n ~
ber 8, 1996
Revlsed version accepted: Adarch 3, 1997